When oceans flood continents, marine incursions often trigger photic zone euxinia (PZE), yet the ecological architecture of these extreme events is not universal. We reveal that the direction of marine incursions fundamentally dictates distinct PZE modes and phototrophic sulfur bacterial ecosystems. By comparing marine incursions in the Eocene Qaidam Basin (China) and the Albian Campos Basin (Brazil), we observed PZE characterized by the proliferation of purple and green sulfur bacteria, respectively. By unlocking sulfurized biomarkers, we capture indigenous molecular fossil signals preserved by natural sulfurization, revealing pristine records of PZE and associated carotenoids. We demonstrate a striking dichotomy of PZE during marine incursions. The 'transgression-restricted basin' type marine incursions in the Qaidam Basin create restricted environments with shallow chemoclines, fostering purple sulfur bacteria dominance. Conversely, the 'transgression-open ocean' type marine incursions in the Campos Basin promote open marine conditions with deep chemoclines, allowing green sulfur bacteria to proliferate. Ultimately, marine incursion trajectories dictate water-column structure and prokaryotic evolution, a dynamic that can only be fully resolved by unlocking sulfurized biomarker archives.